Origin of blood meals in indoor and outdoor resting malaria vectors in western Kenya

AbstractBackgroundUnderstanding the interactions between increased insecticide resistance in field malaria vector populations and the subsequent resting behaviour patterns is important for planning adequate vector control measures in a specific context and sustaining the current vector interventions. The aim of this study was to investigate the resting behavior, host preference and infection with Plasmodium falciparum sporozoites by malaria vectors in different ecological settings of western Kenya with different levels of insecticide resistance.MethodsIndoor and outdoor resting Anopheline mosquitoes were sampled during the dry and rainy seasons in Kisian (lowland site) and Bungoma (highland site), both in western Kenya. WHO tube bioassay was used to determine levels of phenotypic resistance of first generation offspring (F1 progeny) of malaria vectors resting indoors and outdoors to deltamethrin. PCR-based molecular diagnostics were used for mosquito speciation, genotype for resistance mutations and to determine specific host blood meal origins. Enzyme-linked Immunosorbent Assay (ELISA) was used to determine mosquito sporozoite infections.ResultsOverall, 3,566 female Anopheles mosquitoes were collected with Anopheles gambiae s.l [In Bungoma, An. gambiae s.s (90.9%), An arabiensis (7.6%) and in Kisian, An. gambiae s.s (38.9%), An. arabiensis (60.2%)] being the most abundant species (74.7%) followed by An. funestus s.l (25.3%). The majority of An. gambiae s.l (85.4 and 58%) and An. funestus (96.6 and 91.1%) were caught resting indoors in Bungoma and Kisian respectively.Vgsc-1014S was observed at a slightly higher frequency in An. gambiae s.s hereafter(An. gambiae) resting indoor than outdoor (89.7 vs 84.6% and 71.5 vs 61.1%) in Bungoma and Kisian respectively. For An. arabiensis, Vgsc-1014S was 18.2% indoor and outdoor (17.9%) in Kisian. In Bungoma, the Vgsc-1014S was only detected in An. arabiensis resting indoors with a frequency of 10%. The Vgsc-1014F mutation was only present in An. gambiae resting indoors from both sites, but at very low frequencies in Kisian compared to Bungoma (0.8 and 9.2% respectively. In Bungoma, the sporozoite rates for An. funestus, An. gambiae, and An. arabiensis resting indoors were 10.9, 7.6 and 3.4 % respectively. For outdoor resting, An. gambiae and An. arabiensis in Bungoma, the sporozoite rates were 4.7 and 2.9 % respectively.Overall, in Bungoma, the sporozoite rate for indoor resting mosquitoes was 8.6% and 4.2% for outdoors. In Kisian the sporozoite rate was 0.9% for indoor resting An. gambiae. None of the outdoor collected mosquitoes in Kisian tested positive for sporozoite infections.ConclusionThe study reports high densities of insecticide-resistant An. gambiae and An. funestus resting indoors and the persistence of malaria transmission indoors with high entomological inoculation rates (EIR) regardless of the use of Long-lasting insecticidal nets (LLINs). These findings underline the difficulties of controlling malaria vectors resting and biting indoors using the current interventions. Supplemental vector control tools and implementation of sustainable insecticide resistance management strategies are needed in western Kenya.

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Impact of cattle on the abundance of indoor and outdoor resting malaria vectors in southern Malawi

Malaria Journal ◽

10.1186/s12936-021-03885-x ◽

2021 ◽

Vol 20 (1) ◽

Author(s):

Monicah M. Mburu ◽

Kennedy Zembere ◽

Themba Mzilahowa ◽

Anja D. Terlouw ◽

Tumaini Malenga ◽

...

Keyword(s):

Malaria Vector ◽

Blood Meal ◽

Linear Models ◽

Anopheles Funestus ◽

Malaria Vectors ◽

Malaria Vector Control ◽

Previous Night ◽

Outdoor Resting ◽

Blood Meals ◽

Indoor And Outdoor

Abstract Background Understanding the blood feeding preferences and resting habits of malaria vectors is important for assessing and designing effective malaria vector control tools. The presence of livestock, such as cattle, which are used as blood meal hosts by some malaria vectors, may impact malaria parasite transmission dynamics. The presence of livestock may provide sufficient blood meals for the vectors, thereby reducing the frequency of vectors biting humans. Alternatively, the presence of cattle may enhance the availability of blood meals such that infectious mosquitoes may survive longer, thereby increasing the risk of malaria transmission. This study assessed the effect of household-level cattle presence and distribution on the abundance of indoor and outdoor resting malaria vectors. Methods Houses with and without cattle were selected in Chikwawa district, southern Malawi for sampling resting malaria vectors. Prokopack aspirators and clay pots were used for indoor and outdoor sampling, respectively. Each house was sampled over two consecutive days. For houses with cattle nearby, the number of cattle and the distances from the house to where the cattle were corralled the previous night were recorded. All data were analysed using generalized linear models fitted with Poisson distribution. Results The malaria vectors caught resting indoors were Anopheles gambiae sensustricto (s.s.), Anopheles arabiensis and Anopheles funestuss.s. Outdoor collections consisted primarily of An. arabiensis. The catch sizes of indoor resting An. gambiae sensulato (s.l.) were not different in houses with and without cattle (P = 0.34). The presence of cattle near a house was associated with a reduction in the abundance of indoor resting An. funestuss.l. (P = 0.04). This effect was strongest when cattle were kept overnight ≤ 15 m away from the houses (P = 0.03). The blood meal hosts varied across the species. Conclusion These results highlight differences between malaria vector species and their interactions with potential blood meal hosts, which may have implications for malaria risk. Whereas An. arabiensis remained unaffected, the reduction of An. funestuss.s. in houses near cattle suggests a potential protective effect of cattle. However, the low abundance of mosquitoes reduced the power of some analyses and limited the generalizability of the results to other settings. Therefore, further studies incorporating the vectors’ host-seeking behaviour/human biting rates are recommended to fully support the primary finding.

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Insecticide resistance status of indoor and outdoor resting malaria vectors in a highland and lowland site in Western Kenya

10.1101/2020.10.05.326108 ◽

2020 ◽

Author(s):

Kevin O. Owuor ◽

Maxwell G. Machani ◽

Wolfgang R. Mukabana ◽

Stephen Munga ◽

Guiyun Yan ◽

...

Keyword(s):

Insecticide Resistance ◽

Anopheles Gambiae ◽

Sub Saharan Africa ◽

Malaria Vectors ◽

Moderate Intensity ◽

Monooxygenase Activity ◽

Western Kenya ◽

Malaria Mosquitoes ◽

Outdoor Resting ◽

Indoor And Outdoor

AbstractBackgroundLong Lasting Insecticidal Nets (LLINs) and indoor residual spraying (IRS) represent powerful tools for controlling malaria vectors in sub-Saharan Africa. The success of these interventions relies on their capability to inhibit indoor feeding and resting of malaria mosquitoes. This study sought to understand the interaction of insecticide resistance with indoor and outdoor resting behavioral responses of malaria vectors from Western Kenya.MethodsThe status of insecticide resistance among indoor and outdoor resting anopheline mosquitoes was compared in Anopheles mosquitoes collected from Kisumu and Bungoma counties in Western Kenya. The level and intensity of resistance were measured using WHO-tube and CDC-bottle bioassays, respectively. The synergist piperonyl butoxide (PBO) was used to determine if metabolic activity (monooxygenase enzymes) explained the resistance observed. The mutations at the voltage-gated sodium channel (Vgsc) gene and Ace 1 gene were characterized using PCR methods. Microplate assays were used to measure levels of detoxification enzymes if present.ResultsA total of 1094 samples were discriminated within Anopheles gambiae s.l. and 289 within An. funestus s.l. In Kisian (Kisumu county), the dominant species was Anopheles arabiensis 75.2% (391/520) while in Kimaeti (Bungoma county) collections the dominant sibling species was Anopheles gambiae s.s 96.5% (554/574). The An. funestus s.l samples analysed were all An. funestus s.s from both sites. Pyrethroid resistance of An.gambiae s.l F1 progeny was observed in all sites. Lower mortality was observed against deltamethrin for the progeny of indoor resting mosquitoes compared to outdoor resting mosquitoes (Mortality rate: 37% vs 51%, P=0.044). The intensity assays showed moderate-intensity resistance to deltamethrin in the progeny of mosquitoes collected from indoors and outdoors in both study sites. In Kisian, the frequency of vgsc-L1014S and vgsc-L1014F mutation was 0.14 and 0.19 respectively in indoor resting malaria mosquitoes while those of the outdoor resting mosquitoes were 0.12 and 0.12 respectively. The ace 1 mutation was present in higher frequency in the F1 of mosquitoes resting indoors (0.23) compared to those of mosquitoes resting outdoors (0.12). In Kimaeti, the frequencies of vgsc-L1014S and vgsc-L1014F were 0.75 and 0.05 respectively for the F1 of mosquitoes collected indoors whereas those of outdoor resting ones were 0.67 and 0.03 respectively. The ace 1 G119S mutation was present in progeny of mosquitoes from Kimaeti resting indoors (0.05) whereas it was absent in those resting outdoors. Monooxygenase activity was elevated by 1.83 folds in Kisian and by 1.33 folds in Kimaeti for mosquitoes resting indoors than those resting outdoors respectively.ConclusionThe study recorded high phenotypic, metabolic and genotypic insecticide resistance in indoor resting populations of malaria vectors compared to their outdoor resting counterparts. The indication of moderate resistance intensity for the indoor resting mosquitoes is alarming as it could have an operational impact on the efficacy of the existing pyrethroid based vector control tools. The use of synergist (PBO) in LLINs may be a better alternative for widespread use in these regions recording high insecticide resistance.

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Insecticide resistance status of indoor and outdoor resting malaria vectors in a highland and lowland site in Western Kenya

PLoS ONE ◽

10.1371/journal.pone.0240771 ◽

2021 ◽

Vol 16 (3) ◽

pp. e0240771

Author(s):

Kevin O. Owuor ◽

Maxwell G. Machani ◽

Wolfgang R. Mukabana ◽

Stephen O. Munga ◽

Guiyun Yan ◽

...

Keyword(s):

Insecticide Resistance ◽

Anopheles Gambiae ◽

Sub Saharan Africa ◽

Malaria Vectors ◽

Moderate Intensity ◽

Monooxygenase Activity ◽

Western Kenya ◽

Malaria Mosquitoes ◽

Outdoor Resting ◽

Indoor And Outdoor

Background Long Lasting Insecticidal Nets (LLINs) and indoor residual spraying (IRS) represent powerful tools for controlling malaria vectors in sub-Saharan Africa. The success of these interventions relies on their capability to inhibit indoor feeding and resting of malaria mosquitoes. This study sought to understand the interaction of insecticide resistance with indoor and outdoor resting behavioral responses of malaria vectors from Western Kenya. Methods The status of insecticide resistance among indoor and outdoor resting anopheline mosquitoes was compared in Anopheles mosquitoes collected from Kisumu and Bungoma counties in Western Kenya. The level and intensity of resistance were measured using WHO-tube and CDC-bottle bioassays, respectively. The synergist piperonyl butoxide (PBO) was used to determine if metabolic activity (monooxygenase enzymes) explained the resistance observed. The mutations at the voltage-gated sodium channel (Vgsc) gene and Ace 1 gene were characterized using PCR methods. Microplate assays were used to measure levels of detoxification enzymes if present. Results A total of 1094 samples were discriminated within Anopheles gambiae s.l. and 289 within An. funestus s.l. In Kisian (Kisumu county), the dominant species was Anopheles arabiensis 75.2% (391/520) while in Kimaeti (Bungoma county) collections the dominant sibling species was Anopheles gambiae s.s 96.5% (554/574). The An. funestus s.l samples analysed were all An. funestus s.s from both sites. Pyrethroid resistance of An.gambiae s.l F1 progeny was observed in all sites. Lower mortality was observed against deltamethrin for the progeny of indoor resting mosquitoes compared to outdoor resting mosquitoes (Mortality rate: 37% vs 51%, P = 0.044). The intensity assays showed moderate-intensity resistance to deltamethrin in the progeny of mosquitoes collected from indoors and outdoors in both study sites. In Kisian, the frequency of vgsc-L1014S and vgsc-L1014F mutation was 0.14 and 0.19 respectively in indoor resting malaria mosquitoes while those of the outdoor resting mosquitoes were 0.12 and 0.12 respectively. The ace 1 mutation was present in higher frequency in the F1 of mosquitoes resting indoors (0.23) compared to those of mosquitoes resting outdoors (0.12). In Kimaeti, the frequencies of vgsc-L1014S and vgsc-L1014F were 0.75 and 0.05 respectively for the F1 of mosquitoes collected indoors whereas those of outdoor resting ones were 0.67 and 0.03 respectively. The ace 1 G119S mutation was present in progeny of mosquitoes from Kimaeti resting indoors (0.05) whereas it was absent in those resting outdoors. Monooxygenase activity was elevated by 1.83 folds in Kisian and by 1.33 folds in Kimaeti for mosquitoes resting indoors than those resting outdoors respectively. Conclusion The study recorded high phenotypic, metabolic and genotypic insecticide resistance in indoor resting populations of malaria vectors compared to their outdoor resting counterparts. The indication of moderate resistance intensity for the indoor resting mosquitoes is alarming as it could have an operational impact on the efficacy of the existing pyrethroid based vector control tools. The use of synergist (PBO) in LLINs may be a better alternative for widespread use in these regions recording high insecticide resistance.

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Secondary malaria vectors in western Kenya include novel species with unexpectedly high densities and parasite infection rates

Parasites & Vectors ◽

10.1186/s13071-021-04748-9 ◽

2021 ◽

Vol 14 (1) ◽

Author(s):

Amine M. Mustapha ◽

Susan Musembi ◽

Anthony K. Nyamache ◽

Maxwell G. Machani ◽

Jackline Kosgei ◽

...

Keyword(s):

Insecticide Resistance ◽

Malaria Transmission ◽

Malaria Vectors ◽

Malaria Vector Control ◽

Population Declines ◽

Cross Sectional ◽

Western Kenya ◽

Trapping Methods ◽

Unidentified Species ◽

Indoor And Outdoor

Abstract Background Malaria vector control has been implemented chiefly through indoor interventions targeting primary vectors resulting in population declines—pointing to a possible greater proportional contribution to transmission by secondary malaria vectors with their predominant exophagic and exophilic traits. With a historical focus on primary vectors, there is paucity of data on secondary malaria vectors in many countries in Africa. This study sought to determine the species compositions and bionomic traits, including proportions infected with Plasmodium falciparum and phenotypic insecticide resistance, of secondary vectors in three sites with high malaria transmission in Kisumu County, western Kenya. Methods Cross-sectional sampling of adult Anopheles was conducted using indoor and outdoor CDC light traps (CDC-LT) and animal-baited traps (ABTs) in Kakola-Ombaka and Kisian, while larvae were sampled in Ahero. Secondary vectors captured were exposed to permethrin using WHO bioassays and then analyzed by ELISA to test for proportions infected with P. falciparum sporozoites. All Anopheles were identified to species using morphological keys with a subset being molecularly identified using ITS2 and CO1 sequencing for species identification. Results Two morphologically identified secondary vectors captured—An. coustani and An. pharoensis—were determined to consist of four species molecularly. These included An. christyi, An. sp. 15 BSL-2014, an unidentified member of the An. coustani complex (An. cf. coustani) and a species similar to that of An. pharoensis and An. squamosus (An. cf. pharoensis). Standardized (Anopheles per trap per night) capture rates demonstrate higher proportions of secondary vectors across most trapping methods—with overall indoor and outdoor CDC-LTs and ABT captures composed of 52.2% (n = 93), 78.9% (n = 221) and 58.1% (n = 573) secondary vectors respectively. Secondary vectors were primarily caught outdoors. The overall proportion of secondary vectors with P. falciparum sporozoite was 0.63% (n = 5), with the unidentified species An. cf. pharoensis, determined to carry Plasmodium. Overall secondary vectors were susceptible to permethrin with a > 99% mortality rate. Conclusions Given their high densities, endophily equivalent to primary vectors, higher exophily and Plasmodium-positive proportions, secondary vectors may contribute substantially to malaria transmission. Unidentified species demonstrate the need for further morphological and molecular identification studies towards further characterization. Continued monitoring is essential for understanding their temporal contributions to transmission, the possible elevation of some to primary vectors and the development of insecticide resistance. Graphic Abstract

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Targeting malaria vectors through their blood meals for malaria transmission control

10.1603/ice.2016.94825 ◽

2016 ◽

Author(s):

Brian D. Foy

Keyword(s):

Malaria Transmission ◽

Malaria Vectors ◽

Transmission Control ◽

Blood Meals

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Insecticide resistance status of Anopheles arabiensis in irrigated and non-irrigated areas in western Kenya

Parasites & Vectors ◽

10.1186/s13071-021-04833-z ◽

2021 ◽

Vol 14 (1) ◽

Author(s):

Pauline Winnie Orondo ◽

Steven G. Nyanjom ◽

Harrysone Atieli ◽

John Githure ◽

Benyl M. Ondeto ◽

...

Keyword(s):

Insecticide Resistance ◽

Vector Control ◽

Anopheles Arabiensis ◽

Crop Protection ◽

Indoor Residual Spraying ◽

Malaria Vectors ◽

Western Kenya ◽

Animal Protection ◽

Selection Of ◽

Selection Of Resistance

Abstract Background Malaria control in Kenya is based on case management and vector control using long-lasting insecticidal nets (LLINs) and indoor residual spraying (IRS). However, the development of insecticide resistance compromises the effectiveness of insecticide-based vector control programs. The use of pesticides for agricultural purposes has been implicated as one of the sources driving the selection of resistance. The current study was undertaken to assess the status and mechanism of insecticide resistance in malaria vectors in irrigated and non-irrigated areas with varying agrochemical use in western Kenya. Methods The study was carried out in 2018–2019 in Homa Bay County, western Kenya. The bioassay was performed on adults reared from larvae collected from irrigated and non-irrigated fields in order to assess the susceptibility of malaria vectors to different classes of insecticides following the standard WHO guidelines. Characterization of knockdown resistance (kdr) and acetylcholinesterase-inhibiting enzyme/angiotensin-converting enzyme (Ace-1) mutations within Anopheles gambiae s.l. species was performed using the polymerase chain reaction (PCR) method. To determine the agricultural and public health insecticide usage pattern, a questionnaire was administered to farmers, households, and veterinary officers in the study area. Results Anopheles arabiensis was the predominant species in the irrigated (100%, n = 154) area and the dominant species in the non-irrigated areas (97.5%, n = 162), the rest being An. gambiae sensu stricto. In 2018, Anopheles arabiensis in the irrigated region were susceptible to all insecticides tested, while in the non-irrigated region reduced mortality was observed (84%) against deltamethrin. In 2019, phenotypic mortality was decreased (97.8–84% to 83.3–78.2%). In contrast, high mortality from malathion (100%), DDT (98.98%), and piperonyl butoxide (PBO)-deltamethrin (100%) was observed. Molecular analysis of the vectors from the irrigated and non-irrigated areas revealed low levels of leucine-serine/phenylalanine substitution at position 1014 (L1014S/L1014F), with mutation frequencies of 1–16%, and low-frequency mutation in the Ace-1R gene (0.7%). In addition to very high coverage of LLINs impregnated with pyrethroids and IRS with organophosphate insecticides, pyrethroids were the predominant chemical class of pesticides used for crop and animal protection. Conclusion Anopheles arabiensis from irrigated areas showed increased phenotypic resistance, and the intensive use of pesticides for crop protection in this region may have contributed to the selection of resistance genes observed. The susceptibility of these malaria vectors to organophosphates and PBO synergists in pyrethroids offers a promising future for IRS and insecticide-treated net-based vector control interventions. These findings emphasize the need for integrated vector control strategies, with particular attention to agricultural practices to mitigate mosquito resistance to insecticides. Graphic abstract

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